Snapping turtles (Chelydra serpentina) demonstrate temperature-dependent sex determination (TSD): intermediate egg incubation temperatures (23–27 °C) produce males, while extreme temperatures produce females. Snapping turtles are also sexually dimorphic: adult males are typically larger than females. Previous researchers hypothesized that male-producing egg temperatures enhanced the growth rate of juvenile turtles, resulting in the adult dimorphism and potentially providing an adaptive benefit for TSD. In reptiles, the choice of ambient temperature can also influence growth. I measured the effect of egg incubation temperature on juvenile growth rate and water temperature choice of C. serpentina. Eggs were incubated in the laboratory at 21.5, 24.5, 27.5 or 30.5 °C to produce both sexes, all males, both sexes or all females, respectively. Egg temperature was linearly and negatively correlated with growth rate of both male and female juveniles. Thus, growth was enhanced, but not maximized, by male-producing egg temperatures. Egg temperature was also negatively correlated with juvenile temperature choice such that, on average, turtles from 21.5 °C eggs selected 28 °C water, while turtles from 30.5 °C eggs chose 24.5 °C water. Additionally, these temperature choices were highly repeatable, even following a 6 month hibernation period at 7 °C. Thus, while male egg temperatures do not directly maximize growth, multiple effects of embryonic temperature may combine to create long-lasting differences in the behavioral physiology of male and female C. serpentina. Such differences could be important to the ecology and evolution of TSD.

Growth rate and choice of environmental temperature can profoundly influence the ecology and fitness of organisms. In reptiles, temperature choice can affect energy requirements, habitat partitioning, locomotor performance and many aspects of development, physiology and behavior (Huey, 1982; Lillywhite, 1987; Rome et al. 1992; Peterson et al. 1993; Packard and Packard, 1994). In most organisms, growth rate affects life history and can influence total reproductive fitness (Schultz and Warner, 1991; Gotthard et al. 1994; Sedinger et al. 1995). Growth rate and temperature choice are highly plastic in most juvenile and adult animals; for example, both traits vary in response to recent ambient temperatures (Cossins and Bowler, 1987; Hutchinson and Dupré, 1992; Rome et al. 1992). This fact suggests that early developmental temperatures might influence subsequent growth and temperature choice. However, little is known about the embryonic regulation of these traits. The present study examines such regulation in the common snapping turtle Chelydra serpentina.

The consequences of embryonic temperature are particularly germane in reptiles. Reptiles are ectothermic, and both egg-laying and live-bearing species can experience a range of temperatures during embryogenesis. This temperature variance influences many postnatal traits, including sex (Bull, 1983; Janzen and Paukstis, 1991a; Ewert et al. 1994; Lang and Andrews, 1994; Viets et al. 1994), behavior (Gutzke and Crews, 1988; Flores et al. 1994), locomotor performance and survival (Burger, 1989; Van Damme et al. 1992; Janzen, 1995). The effect on sex (temperature-dependent sex determination or TSD) has attracted extensive discussion of its physiological and evolutionary significance. One hypothesis suggests that TSD will co-occur with sexual size dimorphism in reptiles if embryonic temperature determines growth rate in addition to sex (Deeming and Ferguson, 1988, 1989; Janzen and Paukstis, 1991b; Ewert et al. 1994). Chelydra serpentina is a TSD species with adult males that are larger than females (Gibbons and Lovich, 1990; Ernst et al. 1994). In the present study, I examine the hypothesis that male-producing egg temperatures maximize growth rate in Chelydra serpentina.

The growth rate of ectotherms depends strongly on ambient temperature. The choice of ambient temperature affects ectotherm body temperature; body temperature can affect growth by influencing either the rate or efficiency of energy assimilation (Cossins and Bowler, 1987; Sinervo and Adolph, 1989; Rome et al. 1992; Avery et al. 1993; Beaupre et al. 1993a; Elliott et al. 1996). Thermal preference and growth rate are also related because both can increase in response to increased feeding (Andrews, 1982; Lang, 1987; Lillywhite, 1987; Hutchinson and Dupré, 1992; Peterson et al. 1993). Thus, embryonic effects on juvenile growth could be mediated by juvenile temperature choice. No previous study of turtles has examined the effect of embryonic environment on subsequent temperature choice.

In the present study, I measured the separate effects of embryonic temperature and sex on the growth rate and temperature choice of juvenile C. serpentina and examined the interrelationship of choice and growth patterns. Several previous studies examined the effects of egg temperature on turtle growth (Brooks et al. 1991; Etchberger, 1993; Bobyn and Brooks, 1994; Rhen and Lang, 1995; Roosenburg and Kelley, 1996), but the results of these studies differ, and only one study experimentally separated sex and egg temperature effects (Rhen and Lang, 1995). I separate these effects using a design that complements the previous study, which used hormone treatments to produce both sexes at three egg temperatures (Rhen and Lang, 1995). Snapping turtles eggs are viable across a temperature range of 12 °C and produce females at both extremes of the range. I used these traits to produce each sex at three temperatures by incubating eggs at four temperatures that spanned the viable range.

Egg incubation

Eggs were collected in June of 1992 (three clutches) and 1993 (five clutches) from less than 24 h old nests of Chelydra serpentina L. in Whiteside County, Illinois, USA. Eggs were individually numbered, placed in Styrofoam containers with moistened peat moss and transported to the laboratory at the University of Chicago. Eggs were weighed to the nearest 0.1 g, and an equal number (range 4–6) from each clutch was assigned randomly to each of ten (1992) or twelve (1993) plastic boxes (8 cm high × 15 cm wide × 33 cm long) containing moistened vermiculite (−150 kPa ≈ 300 g of dry vermiculite plus 337 g of deionized water) (Janzen et al. 1990). Within each box, 18–27 eggs were randomly assigned to a position in a three by nine matrix and half-buried 1–2 cm apart in the substratum.

In the study population, C. serpentina eggs are generally viable between 20 and 32 °C, produce males between 23 and 27 °C, and produce females above 28 and below 21 °C (F. Janzen, personal communication). The incubation treatments were designed to detect independent and interactive effects of sex and incubation temperature on subsequent measurements. Four constant-temperature (±0.5 °C) incubators were used. The four temperatures, 21.5, 24.5, 27.5 and 30.5 °C, were predicted to produce both sexes, all males, both sexes and all females, respectively. In 1992, two egg boxes were placed at 21.5, 24.5 and 30.5 °C and four boxes at 27.5 °C. In 1993, two boxes were placed at 24.5 and 30.5 °C and four boxes at 21.5 and 27.5 °C. Box positions were shifted in the incubators daily to mitigate the potential effect of thermal gradients on the developing embryos (Bull et al. 1982). To maintain a constant hydric environment, substrata were rehydrated once weekly by adding enough deionized water to return each box, including contents, to its initial mass. The temperatures and hydric conditions used in this experiment are within the range of those measured in natural C. serpentina nests (Packard et al. 1985). Hatching success was greater than 95 % in all treatments.

Hatchling temperature choice and growth rate

On pipping, each egg was isolated in the incubation box by a plastic divider that identified the hatchling. Within 24 h of hatching, turtles were rinsed of vermiculite and adhering membranes, blotted dry and weighed to the nearest 0.1 g. Mid-line carapace length and carapace width at mid-body were measured to the nearest 0.1 mm. Approximately equal numbers of turtles from each of two (1992) or three (1993) clutches were selected at random for the temperature choice and growth experiments. Selected turtles were labeled with an identifying tag visible to a human observer from 1.5 m away. The tags consisted of a labeled 1 cm×1 cm square of thin plastic, secured with dental floss tied through two needle holes in the marginal scutes of the carapace. Turtles were then returned to their original incubators and housed in the incubation boxes on moistened vermiculite. Hatchlings were not fed while housed in the incubators. A 12 h:12 h light:dark cycle (lights on at 07:00 h) was initiated in each incubator when the first hatchling emerged. This 12 h:12 h cycle was maintained throughout the following experiments. Three to six days after hatching, turtles were released into tanks (described below) where temperature choice and growth rate were monitored for 8–16 weeks. In 1992, all the turtles were released into a single large tank, whereas in 1993 the turtles from different incubation treatments were released in separate groups into a set of smaller replicate tanks. These differences between the years are detailed below.

The 1992 experimental design simulated an isolated natural pond in which hatchlings from nests at different temperatures interact during their first year. Cooler incubation temperatures result in longer incubation times. Thus, the age, size, density and history of hatchlings sharing a pond differs among turtles that experience different incubation temperatures. Similarly, the experimental design combined the effects of incubation temperature with those of the resulting social environment. Turtles were released into one tank at time intervals reflecting the differences in incubation time. Twelve turtles from 30.5 °C eggs were released on day 0 (August 14) and removed on day 116. Turtles from 27.5 °C eggs were released in two separate groups of twelve, because of the logistic demands of a companion experiment (O’Steen, 1995). The effect of the division into two groups on all subsequent measurements was examined using analysis of variance (ANOVA). Group had no effect, and the 27.5 °C turtles were treated as one group for subsequent analyses. These two groups were released on day 6 and day 14, and removed on day 123 and day 130, respectively. Turtles from 24.5 °C were released on day 21 and removed on day 138, and turtles from 21.5 °C eggs were released on day 52 and removed on day 168. The tank was 0.75 m wide × 3 m long and was filled to 12 cm with tap water. The tank contained three chambers separated by insulated dividers that the turtles could easily surmount, but that prevented water exchange between the chambers. Aquarium heaters and circulating water pumps kept the water in the three chambers at constant temperatures of 20, 25 and 30±1 °C, respectively. Equal numbers of turtles chosen at random from each treatment group were released into each of the three chambers. Temperature choice was assayed by recording the identity of individual turtles in each chamber once each morning and afternoon, five days a week, every second or third week throughout the experiment. Water temperatures were recorded after each behavior sample using a thermocouple thermometer correct to ±0.1 °C. Mean temperature choice was calculated as the mean temperature of the water inhabited by an individual turtle per week and over the full 16 weeks of the experiment. Turtles were fed daily (after the second behavior sample) the amount of Repto-min that they could consume in less than 10 min. Turtles were weighed to the nearest 0.1 g every 2 weeks. Growth rate was calculated as the slope of the regression of loge(mass) over time, which approximated a straight line (Sinervo and Adolph, 1989).

The 1993 experiment complemented the 1992 design; 1993 hatchlings were raised in a more artificial but standardized social environment. Groups of 14 turtles from the same egg temperature were raised in replicate tanks. Two tanks were used for each egg temperature which produced a single sex (24.5 and 30.5 °C), and three tanks were used for each mixed-sex incubation temperature (21.5 and 27.5 °C). Tanks were 0.75 m wide × 0.75 m long, filled to 12 cm with tap water. Each tank contained two chambers with dividers, as in 1992; water in the two chambers was kept at 20 and 30±1 °C, respectively. The location of individual turtles was recorded twice a day, 5 days a week for 8 weeks following release. Temperature choice was calculated as in 1992. Turtles were fed daily; each tank received 1.5 g of Repto-min for every 100 g of total turtle mass in the tank (calculated using the most recent masses measured). This amount of food was typically consumed in less than 10 min. Turtles were weighed every 2 weeks for 8 weeks. Growth rate was calculated as in the 1992 experiment.

At the end of 8 weeks, the turtle tank groups were moved to a 7 °C room for 6 months (details in O’Steen, 1995). Note that turtle groups entered aestivation on different dates; thus, the relative mass of turtles on particular calendar dates could not be appropriately compared after the start of aestivation. Turtles in all groups lost mass during the 6 months (range 1–10 % of starting mass), a loss similar to that reported for hatchlings recaptured after their first winter in the field (Galbraith et al. 1989). In the laboratory, mortality ranging from 0 to 50 % per tank changed the relative number of turtles per tank. Overall mortality was 25 %, much lower than that reported for hatchling C. serpentina overwintering in natural nests (Obbard and Brooks, 1981a) and at the low end of annual mortality estimates for 1-to 4-year-old Trachemys scripta turtles (Gibbons and Lovich, 1990). At the end of the 6 month period, the turtles were weighed and returned to the temperature choice tanks. Turtle location was recorded twice daily for 2 weeks, and turtles were fed once daily all the Repto-min they could consume in 10 min; all turtles ate and appeared healthy. After 2 weeks, the experiment was terminated. The experiment was not designed to assay post-hibernation growth rate, and this calculation was not made as this final interval provided only two points for a growth rate regression.

Sexing of turtles

The sex of all turtles from 21.5 and 27.5 °C incubation treatments, 45 turtles from 24.5 °C and 36 turtles from 30.5 °C, was determined by visual inspection of the gonads of dissected animals (Yntema, 1976; Janzen et al. 1990). Turtles were killed with an overdose of anesthetic [0.8 ml of 1:1 distilled H2O:Nembutal (sodium pentobarbitol)] injected into the pericardial cavity; they were then dissected and sexed. Dissected turtles were fixed in formalin and preserved in 70 % ethanol. To check the accuracy of the initial sexing procedure, the preserved turtles were sexed separately by F. Janzen and by the author. These latter two assays were conducted blind with respect to incubation temperature; identity tags on the preserved turtles did not identify sex or incubation treatment. Agreement between the three sexing procedures was 100 %. Turtles from 24.5 and 30.5 °C eggs that were not dissected were assumed to be 100 % males and females, respectively, for several reasons. First, all studies of snapping turtle eggs incubated at these and similar temperatures have found 95–100 % single sexes to result (reviewed in Paukstis and Janzen, 1990). Previous studies using the same incubation equipment and population of snapping turtles as the present study found all (25 of 25) 30 °C turtles to be female and all (36 of 36) 26 °C turtles to be male (Janzen, 1995). Finally, in the present study, the 45 dissected turtles from 24.5 °C eggs and 36 turtles from 30.5 °C eggs were all of the predicted sex (males and females, respectively).

Statistical procedures

Data from 1992 and 1993 were analyzed separately because of differences in experimental design. The effects of egg incubation temperature and hatchling sex on hatchling mass, temperature choice and growth rate were examined using separate type III analyses of covariance (ANCOVAs). The type III analyses examine the effect of each variable after removing the effect of all the other variables (Abacus Concepts, 1991). ANCOVAs were generated on a Macintosh computer using SuperANOVA (Abacus Concepts, Berkeley, CA, USA). Egg temperature was tested as a regressor and as a fixed effect in all analyses. Results were equivalent, although treating egg temperature as a regressor always explained a greater portion of the variance. Egg temperature is presented as a regressor for 1992 data, and as a fixed effect for 1993 data, because 1993 tests of tank effects require that incubation temperature be a fixed effect. The other effects included sex, the sex by egg temperature interaction, clutch and egg mass (hatchling mass ANCOVA) or hatchling mass (temperature choice and growth ANCOVAs) as a covariate. The 1993 temperature choice and growth ANCOVAs include tank effects; tank is nested in incubation temperature (see Table 2). Two post-hoc tests were used to define further the relationship between egg temperature and dependent variables. Orthogonal contrasts were used to determine whether the relationship contained linear, quadratic and cubic components (first-, second-and third-order polynomials, respectively). Where needed, Bonferroni/Dunn multiple-comparisons tests were used to compare means among the four egg temperature treatments.

The repeatability of temperature choice was determined by calculating Kendall’s coefficient of concordance (W) for the egg temperature groups and for individuals within groups (Sokal and Rohlf, 1981). W derives from rank orderings and so provides a measure of repeatability relative to the other individuals or groups in the calculation. Weekly means of temperature choice (10 choices per turtle per week) were used for the calculations. In 1992, W was calculated across the 16 week monitoring period using every second-weekly mean. In 1993, W was calculated over two intervals, first using all eight means from the first 8 weeks after hatching, and then using weeks 7 and 8 and the two weekly means following the 6 month laboratory wintering period.

Sex ratio

Egg incubation temperatures of 21.5 and 27.5 °C produced mixed sex ratios in both years, as predicted. The 21.5 °C incubations produced 18 males and five females in 1992, and 18 males and 23 females in 1993. The 27.5 °C incubations produced 22 males and 32 females in 1992, and 25 males and 15 females in 1993. Sexed turtles from 24.5 and 30.5 °C incubations were all males and all females, respectively. The tables and figures present the sex ratios of turtles used in individual experiments, where appropriate.

Hatchling mass

Within each year, hatchlings from high and low egg incubation temperatures weighed less than hatchlings from intermediate temperatures (Table 1). ANCOVAs for each year indicated that egg temperature, clutch and egg mass explained the variance for hatchling mass (P<0.0001, P<0.02, P<0.0001, respectively), while sex and the interaction between sex and egg temperature did not (P>0.26, P>0.14, respectively). Orthogonal contrasts further defined the effect of egg temperature on hatchling mass. These analyses indicated that a quadratic (second-order polynomial) relationship existed in both years (P<0.0001) and that a positive linear relationship also existed in 1993 (P=0.0001).

Table 1.

Mass of hatchling snapping turtles incubated at different temperatures

Mass of hatchling snapping turtles incubated at different temperatures
Mass of hatchling snapping turtles incubated at different temperatures

Despite these differences among egg temperatures, hatchling mass had no effect on subsequent growth rate or temperature choice (Table 2). Indeed, the pattern of the effect of egg temperature on hatchling mass differed from the pattern for growth rate and temperature choice (see below), and differences in hatchling mass were negligible compared with the effects of growth rate and hatching date on relative juvenile size (see Discussion and Fig. 4).

Table 2.

ANCOVA results for growth rate and temperature choice of juvenile turtles

ANCOVA results for growth rate and temperature choice of juvenile turtles
ANCOVA results for growth rate and temperature choice of juvenile turtles

Hatchling growth rate

Turtles from cooler egg incubation temperatures grew faster than those from warmer egg temperatures in both years of the study (Fig. 1; Table 2). Notably, egg temperature was the only factor that affected growth rate (Table 2), and the temperature effect did not differ between the sexes (Table 2, interaction term). Orthogonal contrasts indicated that the egg temperature effect was linear in both years (P<0.002) and had no quadratic (P>0.34) or cubic (P>0.26) components in either year. Accordingly, the highest average growth rates occurred in the mixed-sex groups of turtles from 21.5 °C eggs, and these rates were not significantly different from those of the all-male groups of turtles from 24.5 °C eggs (Fig. 1; overall mean difference = 0.007loge(g) week−1, P=0.42, Bonferroni/Dunn). In 1992, but not in 1993, the separate effects of egg temperature on sex ratio and growth rate created a small difference in the overall average growth rate of the sexes; males grew slightly faster (data from Fig. 1; 1992 mean difference = 0.021loge(g) week−1, t=2.6, P=0.01; 1993 mean difference = 0.005loge(g) week−1, t=0.62, P=0.54). These results derive from the specific egg temperatures used and the number of eggs incubated at each temperature. Thus, if egg temperature affects hatchling growth in nature, any resulting difference between the sexes will depend on the distribution of nest sizes and temperatures.

Fig. 1.

Egg incubation temperature was negatively correlated with subsequent growth rates of male and female snapping turtles (statistics are given in Table 2 and the Results). Growth rate was calculated as the slope of the regression of loge(mass) (in g) over time (in weeks) calculated over the first 16 weeks after hatching in 1992 and the first 8 weeks after hatching in 1993. Values are means + S.E.M.; values of N are given within the columns. Different time intervals produced equivalent results (data not shown).

Fig. 1.

Egg incubation temperature was negatively correlated with subsequent growth rates of male and female snapping turtles (statistics are given in Table 2 and the Results). Growth rate was calculated as the slope of the regression of loge(mass) (in g) over time (in weeks) calculated over the first 16 weeks after hatching in 1992 and the first 8 weeks after hatching in 1993. Values are means + S.E.M.; values of N are given within the columns. Different time intervals produced equivalent results (data not shown).

Hatchling temperature choice

Egg temperature strongly affected the water temperature choice of juvenile turtles. In both sexes, temperature choice was negatively correlated with egg temperature, such that turtles from 21.5 °C eggs selected water 3.5 °C warmer on average than turtles from 30.5 °C eggs (Fig. 2; Table 2). This effect occurred in both years of the study, despite differences in social and physical environments. Orthogonal contrasts confirmed that a linear effect of egg temperature occurred in both years (P=0.0001) and also indicated a cubic effect (P=0.03) in 1992. These patterns, combined with the number of eggs placed at each temperature and the effects of egg temperature on sex ratio, resulted in juvenile males choosing warmer temperatures overall than females (1992 mean difference 1.2 °C, t=2.6, P=0.01; 1993 mean difference 0.7 °C, t=1.4, P=0.15).

Fig. 2.

Increasing egg incubation temperatures resulted in decreasing water temperature choice among juvenile turtles of both sexes. Water temperature is highly positively correlated with body temperature in field studies of snapping turtles (Punzo, 1975; Obbard and Brooks, 1981b), and temperature choice is assumed to reflect body temperature here. Temperature choice was averaged over the first 16 and 8 weeks after hatching in 1992 and 1993, respectively. Statistics are presented in Table 2 and the Results. Sample sizes are as in Fig. 1. Values are means + S.E.M.

Fig. 2.

Increasing egg incubation temperatures resulted in decreasing water temperature choice among juvenile turtles of both sexes. Water temperature is highly positively correlated with body temperature in field studies of snapping turtles (Punzo, 1975; Obbard and Brooks, 1981b), and temperature choice is assumed to reflect body temperature here. Temperature choice was averaged over the first 16 and 8 weeks after hatching in 1992 and 1993, respectively. Statistics are presented in Table 2 and the Results. Sample sizes are as in Fig. 1. Values are means + S.E.M.

Notably, temperature choices were highly consistent among egg temperature groups and among most individuals (Table 3). Turtles even retained their temperature choice ranks after 6 months at 7 °C, despite changing their absolute temperature choices (Table 3; Fig. 3). Among the turtles that survived hibernation, mean selected temperature increased by 1.4 °C (repeated-measures ANCOVA, F=22.2, P=0.0001), and the increase did not differ between incubation groups or between the sexes (F=1.0, P=0.43 for incubation group; F=0.1, P=0.99 for sex). Individuals from only two groups, 1992 turtles from 24.5 °C eggs and 1993 turtles from 21.5 °C eggs, did not show significant temperature choice concordance (W) (Table 3). However, as W derives from rank orderings, this lack of significance may be due to the low variance in temperature choice in these groups (Fig. 3) rather than to the lack of intra-individual repeatability. Low choice variance resulted as all individuals in these groups spent most of their time at the highest water temperature available (data not shown).

Table 3.

Kendall’s coefficients of concordance (W) for the weekly mean temperature choice of individuals and groups

Kendall’s coefficients of concordance (W) for the weekly mean temperature choice of individuals and groups
Kendall’s coefficients of concordance (W) for the weekly mean temperature choice of individuals and groups
Fig. 3.

The effects of egg incubation temperature on juvenile temperature choice persisted over time. Turtles maintained consistent relative temperature choices before and after the laboratory wintering period, despite increasing their absolute temperature choices after the winter (Results, see Table 3 for statistics). Weekly temperature choices represent the means of 10 choices per turtle per week. Data from females and males did not differ significantly; sexes are combined in the graph. The data include only 1993 turtles that survived overwintering. Data from 1992 showed similar consistency (Table 3). Values are means + S.E.M.

Fig. 3.

The effects of egg incubation temperature on juvenile temperature choice persisted over time. Turtles maintained consistent relative temperature choices before and after the laboratory wintering period, despite increasing their absolute temperature choices after the winter (Results, see Table 3 for statistics). Weekly temperature choices represent the means of 10 choices per turtle per week. Data from females and males did not differ significantly; sexes are combined in the graph. The data include only 1993 turtles that survived overwintering. Data from 1992 showed similar consistency (Table 3). Values are means + S.E.M.

Effects of egg incubation temperature on hatchling growth

The sexual dimorphism hypothesis suggests that adult male snapping turtles are larger than females in nature because male egg temperatures enhance growth (Deeming and Ferguson, 1988, 1989). The present results suggest that this hypothesis is partly correct, but that multiple factors contribute to size dimorphism. In this study, male egg temperatures enhanced, but did not maximize, growth rates. In the study population, 23–27 °C eggs produce males. Yet the growth rate of turtles from 21.5 °C eggs was not significantly different from that of turtles from 24.5 °C eggs (see Results). Overall, growth rates were linearly and negatively correlated with egg incubation temperatures (Fig. 1, see Results). This result is unique; previous findings are more consistent with the hypothesis. Bobyn and Brooks (1994), Brooks et al. (1991) and McKnight and Gutzke (1993) report high growth rates in hatchling C. serpentina from eggs incubated at intermediate temperatures (25.5–27 °C) and low growth rates in hatchlings from eggs incubated at extreme temperatures (22 °C and 28.6–31 °C). Rhen and Lang (1995) found that snapping turtles from both 24 and 26.5 °C eggs grew faster than turtles from 29 °C eggs. Rhen and Lang (1995) did not study an extreme low egg temperature, and so their results are consistent both with mine and with the sexual dimorphism hypothesis.

One factor, access to a thermal gradient, may explain the different results of these studies. Snapping turtles displaying a curvilinear relationship between egg temperature and growth rate were raised at uniform temperatures (21–25 °C) (Brooks et al. 1991; McKnight and Gutzke, 1993; Bobyn and Brooks, 1994). Turtles showing linear or potentially linear relationships between growth rate and egg temperature had access to thermal gradients of at least 21–30 °C (this study, Rhen and Lang, 1995). Thus, high growth rates of juvenile C. serpentina from low egg temperatures (below 24 °C) may depend on the ability to select high temperatures behaviorally. This conclusion is supported by many studies that find differing growth rates between reptiles in thermal gradients and those in constant-temperature environments (e.g. Lang, 1987; Sinervo and Adolph, 1989; Denver and Licht, 1991). Turtles inhabit thermal gradients in nature; thus, hatchlings from cool nests may have maximal growth rates if warm temperatures are available.

Interestingly, negative correlations between growth rate and egg temperature are not reported in other turtles. The diamondback terrapin (Malaclemys terrapin) displays a positive correlation between egg temperature and hatchling growth rate (Roosenburg and Johnson, 1995; Roosenburg and Kelley, 1996), while the loggerhead musk turtle (Sternotherus minor) displays no correlation (Etchberger, 1993). These studies did not specify sex effects or juvenile thermal environments; these factors may help to explain the divergent patterns. Divergent patterns also appear in other reptiles. In crocodilian studies, for example, Joanen et al. (1987) report that extreme egg temperatures reduce growth rate in juvenile Alligator mississippiensis raised in constant-temperature environments, yet Webb and Cooper-Preston (1989) report a positive correlation between egg temperature and growth rate of juvenile Crocodylus porosus raised in a thermal gradient. Clearly, detecting any broad patterns of relationship between embryonic temperature and juvenile growth rate in reptiles may require allowing and measuring juvenile temperature choice.

Another factor that may affect juvenile size dimorphism in reptiles is hatching date. Egg incubation temperature affects incubation time; the warmest eggs hatch first (e.g. Yntema, 1978). In the present study, the late hatching date of turtles from 21.5 °C eggs caused these animals to be smaller than the others during most of the study, despite high growth rates (Fig. 4). In contrast, hatching-date-induced size differences among the other turtles disappeared by the time the natural population typically enters hibernation (approximately day 70), and size thereafter diverged according to relative growth rates (Fig. 4). As a result of these patterns, turtles from 24.5 °C eggs may stay larger than turtles from 21.5 °C eggs for several seasons and may be larger than turtles from warmer eggs in adulthood. This possibility awaits testing; it was beyond the scope of the present study to determine whether early size or growth rate differences persist beyond the first hibernation (see Materials and methods).

Fig. 4.

Hatching date affected the relative mass of juvenile turtles. Turtles from 30.5 °C eggs hatched first, in early August. Higher growth rates of turtles from later-hatching, cooler eggs resulted in size convergence of turtles from 24.5, 27.5 and 30.5 °C eggs near the date that the natural population typically enters hibernation (late October, day 70) (Obbard and Brooks, 1981b; Meeks and Ultsch, 1990). However, the extremely late hatching date of 21.5 °C eggs left these turtles smaller at day 70. The relative mass of the different groups could change as depicted by the extrapolated lines if relative growth rates persisted after hibernation (not tested here). The slopes of the regression lines equal the growth rates presented in Fig. 1. Points represent means for each measurement date, with samples sizes as in Fig. 1.

Fig. 4.

Hatching date affected the relative mass of juvenile turtles. Turtles from 30.5 °C eggs hatched first, in early August. Higher growth rates of turtles from later-hatching, cooler eggs resulted in size convergence of turtles from 24.5, 27.5 and 30.5 °C eggs near the date that the natural population typically enters hibernation (late October, day 70) (Obbard and Brooks, 1981b; Meeks and Ultsch, 1990). However, the extremely late hatching date of 21.5 °C eggs left these turtles smaller at day 70. The relative mass of the different groups could change as depicted by the extrapolated lines if relative growth rates persisted after hibernation (not tested here). The slopes of the regression lines equal the growth rates presented in Fig. 1. Points represent means for each measurement date, with samples sizes as in Fig. 1.

To affect adult dimorphism, juvenile size or growth differences would need to persist through maturity, which in snapping turtles takes 4–19 years (Ernst et al. 1994). Alternatively, or additionally, egg temperature could affect adult dimorphism by influencing the differential persistence of growth rates. In a study of natural populations in Iowa, male and female hatchling snapping turtles grew at similar average rates (Christiansen and Burken, 1979), as was found in the present study (see Results). However, in nature, female growth rates declined before male rates, such that males grew faster than females for turtles aged 5–7 years (Christiansen and Burken, 1979). The physiological and ecological mechanisms that create adult sexual size dimorphism in snapping turtles may be fascinatingly complex and remain incompletely known.

Nonetheless, the present study identified physiological and behavioral factors that can contribute to sexual size dimorphism among juvenile C. serpentina. The negative correlations between egg temperature and juvenile growth rate, and between egg temperature and juvenile temperature choice (also see below), could create dimorphism when combined with patterns of availability and choice of nest temperatures in a natural population. For example, if nest temperatures below 24 °C were either rarely available or rarely selected by females, then the resulting male hatchlings might, on average, select warmer water and grow faster than females. This scenario is of interest because it allows behavioral mediation of sexual size dimorphism within a population. Both the nest site choice by females and the temperature choice of hatchlings could mediate the relative growth rates of the sexes. The effect of natural nest temperatures on juvenile growth rates and temperature choice is the subject of a current study.

Effects of egg incubation temperature on hatchling temperature choice

In this study, egg temperature had a strong and long-lasting influence on the temperature choice of juvenile snapping turtles, and this influence was the same in both sexes. This study is the first to report on this relationship in turtles. Two previous studies of reptiles examined this relationship, and they suggest that embryonic temperature does not necessarily dictate temperature choice. In live-bearing Thamnophis elegans garter snakes, maternal temperature during pregnancy does not affect juvenile temperature selection (Arnold et al. 1995). In contrast, Lang (1987) found that either egg temperature or sex was correlated with temperature choice in Crocodylus siamensis, a TSD species. Four male hatchlings from 33 °C eggs selected temperatures on average 3.3 °C higher than two females from 28 °C eggs (Lang, 1987). In the present study, male snapping turtles also selected higher temperatures on average than did females. Interestingly, egg temperature is positively correlated with temperature choice in crocodiles, but negatively correlated in snapping turtles. Males choose higher temperatures in both species because egg temperature has opposite effects on sex in the two species. Thus, either the mechanistic relationship between egg temperature and temperature choice is different in crocodiles and snapping turtles or, in crocodiles, sex has a predominant influence on temperature choice.

Tank group also affected temperature choice in C. serpentina (Table 2). In 1993, turtles were grouped by egg temperature and the groups were raised in replicate tanks (see Materials and methods). The tank effect indicates that either the social groups or the physical traits of the different tanks influenced temperature choice. The former is more likely, as all the tanks had the same physical structures and water temperature profiles, while social factors are known to affect thermoregulatory behavior in a number of ectotherms (reviewed in Lang, 1987). I did not test for social effects experimentally, but several factors indicate that the influence of egg temperature on hatchling temperature choice is robust to social and abiotic effects. First, incubation temperature effects are highly significant even when tank effect is controlled for (Table 2). Second, egg temperature was negatively correlated with hatchling temperature choice in both 1992 and 1993, despite differences in the social and physical environments. Finally, the influence of egg temperature on hatchling temperature choice remained after overwinter mortality had changed the size and composition of social groups (Fig. 3; Table 3).

The ANCOVA also indicated that temperature choice varies between clutches (Table 2). Clutch effects occurred only in 1992, yet they show that maternal or genetic factors can influence juvenile turtle temperature choice. This study did not include sufficient clutches to quantify genetic relationships. However, the availability and large size of C. serpentina clutches lend them to research on genetic correlations and genotype by environment interactions (Janzen, 1992; Rhen and Lang, 1995). The potentially broad importance of temperature choice could make such studies worthwhile.

Relationship between temperature choice and growth rate

Egg temperature had similar effects on growth rate and temperature choice in the present study. This result is unsurprising in that growth and temperature choice are interrelated in reptiles; selecting higher temperatures can increase growth rate, and increased feeding can increase both growth rate and temperature choice (Lang, 1987; Lillywhite, 1987; Rome et al. 1992; Avery et al. 1993; Beaupre et al. 1993a). The present study did not separate feeding, growth and temperature choice experimentally. However, several points suggest that the primary effect of egg temperature was on temperature choice and that choice mediated growth rate. First, as discussed earlier, the growth rate of C. serpentina is not a necessary function of egg temperature; instead, egg temperature effects can be mediated by access to a thermal gradient.

Second, feeding does not increase the temperature chosen by snapping turtles. A laboratory study of juveniles found a negative effect (Knight et al. 1990), and a study of adults in the wild found no effect, of feeding on temperature choices of C. serpentina (Brown and Brooks, 1991). Additionally, feeding rate does not necessarily dictate growth rate. In the second year of the present study, I limited food to a proportion of the total turtle mass in a given tank, recalculated every 2 weeks. Initial turtle masses did not differ across tanks and treatments, and the food was all consumed. Thus, turtles from all incubation temperatures initially consumed similar amounts of food, yet growth rates still diverged.

Finally, ANCOVA supports the prediction that the effects of egg temperature on growth rate result from their effects on temperature choice. ANCOVAs for growth and choice were constructed using the reciprocal traits as covariates (Table 4). The results show that egg temperature affected temperature choice even when the effects of growth rate on choice were removed. In contrast, growth rate was not affected by egg temperature when the effects of temperature choice on growth rate were removed (Table 4). These analyses obviously do not determine cause and effect, but are nonetheless consistent with the prediction.

Table 4.

ANCOVAs of growth rate and temperature choice, including these traits as covariates

ANCOVAs of growth rate and temperature choice, including these traits as covariates
ANCOVAs of growth rate and temperature choice, including these traits as covariates

Importance of temperature choice

Embryonic effects on subsequent temperature choice may be broadly important as, in addition to growth, these effects could impact on a variety of physiological, ecological and evolutionary factors. This potential importance is strengthened by the repeatability of relative temperature choices. Both individuals and groups of turtles maintained stable relative choices throughout this study (Table 3; Fig. 3). Notably, turtles maintained their relative choices even while increasing their absolute temperature choices after hibernation. If such radical temperature changes in the juvenile environment do not override the effects of embryonic temperature, then differences in temperature choice may persist well beyond the life stages assayed here. In other reptiles, egg temperatures can permanently affect several traits, including sex (Bull, 1987) and aggressive and reproductive behaviors (Gutzke and Crews, 1988; Flores et al. 1994) and have long-lasting effects on other traits including growth rate (Joanen et al. 1987; Webb and Cooper-Preston, 1989) and locomotor behaviors (Burger, 1989). In contrast, the effects of temperature acclimation during later life stages are typically reversible. For example, thermal acclimation of critical thermal maxima can be reversed in 3 weeks in juvenile C. serpentina (Williamson et al. 1989), and acclimation of thermal preferences is typically reversible within several months in many adult reptiles (Lillywhite, 1987; Tsuji, 1988; Rome et al. 1992). The present study indicates that, in C. serpentina, embryonic effects on temperature choice may persist much longer than, and in spite of, the effects of temperature on later life stages.

Long-lasting embryonic effects on temperature choice could impact broadly on turtle physiology, ecology and fitness if these effects occur in nature. In addition to affecting growth, temperature choice might affect energy requirements, locomotor performance, habitat choice and other traits (Huey, 1982; Lang, 1987; Lillywhite, 1987; Rome et al. 1992; Beaupre et al. 1993b; Peterson et al. 1993; Sinervo and Adolph, 1994). Furthermore, the distribution of nest sizes and temperatures could result in male and female turtles that differ in these traits. For example, males from cooler nests might occupy the warmer shallow edges of a pond, while females from warmer nests might occupy cooler deeper water, thus exposing the sexes to differential predation risks, food sources, retreat and hibernation sites. If found, such sex differences would support an adaptive basis for the evolution of TSD (Bull, 1983, 1989; Deeming and Ferguson, 1989; Janzen and Paukstis, 1991b; Ewert et al. 1994; Roosenburg, 1996).

I would like to thank S. Arnold, L. Diamond, J. Gladstone and F. Janzen for invaluable technical assistance, and S. Arnold, A. Bennett, B. Block, M. Feder, F. Janzen, J. McLister, M. Wade and an anonymous reviewer for helpful comments on the manuscript. This work was supported in part by an NSF Graduate Fellowship, PHS Genetics Training Grant GMO7197-19 and NSF Grant BSR 91-19588 to S. Arnold.

Abacus Concepts
(
1991
).
SuperANOVA Manual
.
Berkeley, CA
:
Abacus Concepts, Inc
.
Andrews
,
R. M.
(
1982
).
Patterns of growth in reptiles
.
In Biology of the Reptilia
, vol.
13
(ed.
C.
Gans
and
F. H.
Pough
), pp.
273
320
.
London
:
Academic Press
.
Arnold
,
S. J.
,
Peterson
,
C. R.
and
Gladstone
,
J.
(
1995
).
Behavioral variation in natural populations. VII. Maternal body temperature does not affect juvenile thermoregulation in a garter snake (Thamnophis elegans)
.
Anim. Behav
.
50
,
623
633
.
Avery
,
H. W.
,
Spotila
,
J. R.
,
Congdon
,
J. D.
,
Fischer
,
R. U.
, Jr
,
Standora
,
E. A.
and
Avery
,
S. B.
(
1993
).
Role of diet protein and temperature in the growth and nutritional energetics of juvenile slider turtles, Trachemys scripta
.
Physiol. Zool
.
66
,
902
925
.
Beaupre
,
S. J.
,
Dunham
,
A. E.
and
Overall
,
K. L.
(
1993a
).
The effects of consumption rate and temperature on apparent digestibility coefficient, urate production, metabolizable energy coefficient and passage time in canyon lizards (Sceloporus merriami) from two populations
.
Funct. Ecol
.
7
,
273
280
.
Beaupre
,
S. J.
,
Dunham
,
A. E.
and
Overall
,
K. L.
(
1993b
).
Metabolism of a desert lizard: the effects of mass, sex, population of origin, temperature, time of day and feeding on oxygen consumption of Sceloporus merriami
.
Physiol. Zool
.
66
,
128
147
.
Bobyn
,
M. L.
and
Brooks
,
R. J.
(
1994
).
Interclutch and interpopulation variation in the effects of incubation conditions on sex, survival and growth of hatchling turtles (Chelydra serpentina)
.
J. Zool., Lond
.
233
,
233
257
.
Brooks
,
R. J.
,
Bobyn
,
M. L.
,
Galbraith
,
D. A.
,
Layfield
,
J. A.
and
Nancekivell
,
E. G.
(
1991
).
Maternal and environmental influences on growth and survival of embryonic and hatchling snapping turtles (Chelydra serpentina)
.
Can. J. Zool
.
69
,
2667
2676
.
Brown
,
G. P.
and
Brooks
,
R. J.
(
1991
).
Thermal and behavioral responses to feeding in free-ranging turtles, Chelydra serpentina
.
J. Herpetol
.
25
,
273
278
.
Bull
,
J. J.
(
1983
).
Evolution of Sex Determining Mechanisms
.
Menlo Park, CA
:
Benjamin/Cummings
.
Bull
,
J. J.
(
1987
).
Temperature-dependent sex determination in reptiles: validity of sex diagnosis in hatchling lizards
.
Can. J. Zool
.
65
,
1421
1424
.
Bull
,
J. J.
(
1989
).
Evolution and variety of sex-determining mechanisms in amniote vertebrates
.
In Evolutionary Mechanisms in Sex Determination
(ed.
S. S.
Wachtel
), pp.
57
65
.
Boca Raton, FL
:
CRC Press
.
Bull
,
J. J.
,
Vogt
,
R. C.
and
Bulmer
,
M. G.
(
1982
).
Heritability of sex ratio in turtles with environmental sex determination
.
Evolution
36
,
333
341
.
Burger
,
J.
(
1989
).
Incubation temperature has long-term effects on behavior of young pine snakes (Pituophis melanoleucus)
.
Behav. Ecol. Sociobiol
.
24
,
201
207
.
Christiansen
,
J. L.
and
Burken
,
R. R.
(
1979
).
Growth and maturity of the snapping turtle (Chelydra serpentina) in Iowa
.
Herpetologica
35
,
261
266
.
Cossins
,
A. R.
and
Bowler
,
K.
(
1987
).
Temperature Biology of Animals
.
New York
:
Chapman & Hall
.
Deeming
,
D. C.
and
Ferguson
,
M. W. J.
(
1988
).
Environmental regulation of sex determination in reptiles
.
Phil. Trans. R. Soc. Lond. B
322
,
19
39
.
Deeming
,
D. C.
and
Ferguson
,
M. W. J.
(
1989
).
The mechanism of temperature dependent sex determination in crocodilians: a hypothesis
.
Am. Zool
.
29
,
973
985
.
Denver
,
R. J.
and
Licht
,
P.
(
1991
).
Dependence of body growth on thyroid activity in turtles
.
J. exp. Zool
.
258
,
48
59
.
Elliott
,
J. M.
,
Hurley
,
M. A.
and
Allonby
,
J. D.
(
1996
).
A functional model for maximum growth of immature stone loach, Barbatula barbatula, from three populations in north-west England
.
Freshwater Biol
.
36
,
547
554
.
Ernst
,
C. H.
,
Barbour
,
R. W.
and
Lovich
,
J. E.
(
1994
).
Turtles of the United States and Canada
.
Washington DC
:
Smithsonian Institution Press
.
Etchberger
,
C. R.
(
1993
).
The effects of incubation temperature and clutch on post-hatching growth in the loggerhead musk turtle, Sternotherus minor minor
.
Am. Zool
.
33
,
41A
.
Ewert
,
M. A.
,
Jackson
,
D. R.
and
Nelson
,
C. E.
(
1994
).
Patterns of temperature-dependent sex determination in turtles
.
J. exp. Zool
.
270
,
3
15
.
Flores
,
D.
,
Tousignant
,
A.
and
Crews
,
D.
(
1994
).
Incubation temperature affects the behavior of adult leopard geckos (Eublepharis macularius)
.
Physiol. Behav
.
55
,
1067
1072
.
Galbraith
,
D. A.
,
Brooks
,
R. J.
and
Obbard
,
M. E.
(
1989
).
The influence of growth rate on age and body size at maturity in female snapping turtles (Chelydra serpentina)
.
Copeia
1989
,
896
904
.
Gibbons
,
J. W.
and
Lovich
,
J. E.
(
1990
).
Sexual dimorphism in turtles with emphasis on the slider turtle (Trachemys scripta)
.
Herpetol. Monogr
.
4
,
1
29
.
Gotthard
,
K.
,
Nylin
,
S.
and
Wiklund
,
C.
(
1994
).
Adaptive variation in growth rate: life history costs and consequences in the speckled wood butterfly, Pararge aegeria
.
Oecologia
99
,
281
289
.
Gutzke
,
W. H. N.
and
Crews
,
D.
(
1988
).
Embryonic temperature determines adult sexuality in a reptile
.
Nature
332
,
832
834
.
Huey
,
R. B.
(
1982
).
Temperature, physiology and the ecology of reptiles
.
In Biology of the Reptilia
, vol.
12
(ed.
C.
Gans
and
F. H.
Pough
), pp.
25
91
.
London
:
Academic Press
.
Hutchinson
,
V. H.
and
Dupré
,
R. K.
(
1992
).
Thermoregulation
.
In Environmental Physiology of the Amphibians
(ed.
M. E.
Feder
and
W. W.
Burggren
), pp.
206
249
.
Chicago
:
University of Chicago Press
.
Janzen
,
F. J.
(
1992
).
Heritable variation for sex ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina)
.
Genetics
131
,
155
161
.
Janzen
,
F. J.
(
1995
).
Experimental evidence for the evolutionary significance of temperature-dependent sex determination
.
Evolution
49
,
864
873
.
Janzen
,
F. J.
,
Packard
,
G. C.
,
Packard
,
M. J.
,
Boardman
,
T. J.
and
Zumbrunnen
,
J. R.
(
1990
).
Mobilization of lipid and protein by embryonic snapping turtles in wet and dry environments
.
J. exp. Zool
.
255
,
155
162
.
Janzen
,
F. J.
and
Paukstis
,
G. L.
(
1991a
).
Environmental sex determination in reptiles: ecology, evolution and experimental design
.
Q. Rev. Biol
.
66
,
149
179
.
Janzen
,
F. J.
and
Paukstis
,
G. L.
(
1991b
).
A preliminary test of the adaptive significance of environmental sex determination in reptiles
.
Evolution
45
,
435
440
.
Joanen
,
T.
,
Mcnease
,
L.
and
Ferguson
,
M. J. W.
(
1987
).
The effects of egg incubation temperature on post-hatching growth of American alligators
.
In Wildlife Management: Crocodiles and Alligators
(ed.
G. J. W.
Webb
,
S. C.
Manolis
and
P. J.
Whitehead
), pp.
533
537
.
Chirping Norton, Australia
:
Surrey Beatty & Sons
.
Knight
,
T. W.
,
Layfield
,
J. A.
and
Brooks
,
R. J.
(
1990
).
Nutritional status and mean selected temperature of hatchling snapping turtles (Chelydra serpentina): is there a thermophilic response to feeding?
Copeia
1990
,
1067
1072
.
Lang
,
J. W.
(
1987
).
Crocodilian thermal selection
.
In Wildlife Management: Crocodiles and Alligators
(ed.
G. J. W.
Webb
,
S. C.
Manolis
and
P. J.
Whitehead
), pp.
310
317
.
Chirping Norton, Australia
:
Surrey Beatty & Sons
.
Lang
,
J. W.
and
Andrews
,
H. V.
(
1994
).
Temperature-dependent sex determination in crocodilians
.
J. exp. Zool
.
270
,
28
44
.
Lillywhite
,
H. B.
(
1987
).
Temperature, energetics and physiological ecology
.
In Snakes: Ecology and Evolutionary Biology
(ed.
R. A.
Seigel
,
J. T.
Collins
and
S. S.
Novak
), pp.
422
477
.
New York
:
Macmillan
.
Linnaeus
,
C.
(
1758
).
Systema naturae
. 10th edn, pp.
1
824
.
Holmiae, Sweden
.
Mcknight
,
C. M.
and
Gutzke
,
W. H. N.
(
1993
).
Effects of embryonic environment and of hatchling housing conditions on growth of young snapping turtles (Chelydra serpentina)
.
Copeia
1993
,
475
482
.
Meeks
,
R. L.
and
Ultsch
,
G. R.
(
1990
).
Overwintering behavior of snapping turtles
.
Copeia
1990
,
880
884
.
O’steen
,
S.
(
1995
).
Evolutionary physiology of energy use in reptiles
.
PhD thesis
,
University of Chicago
,
Chicago, IL
.
Obbard
,
M. E.
and
Brooks
,
R. J.
(
1981a
).
Fate of overwintered clutches of the common snapping turtle (Chelydra serpentina) in Algonquin Park, Ontario
.
Can. Field-Nat
.
95
,
350
352
.
Obbard
,
M. E.
and
Brooks
,
R. J.
(
1981b
).
A radio-telemetry and mark–recapture study of activity in the common snapping turtle, Chelydra serpentina
.
Copeia
1981
,
630
637
.
Packard
,
G. C.
,
Boardman
,
T. J.
and
Gutzke
,
W. H. N.
(
1985
).
Daily and seasonal variation in hydric conditions and temperature inside nests of common snapping turtles (Chelydra serpentina)
.
Can. J. Zool
.
63
,
2422
2429
.
Packard
,
G. C.
and
Packard
,
M. J.
(
1994
).
The physiological ecology of reptilian eggs and embryos
.
In Biology of the Reptilia
, vol.
16
(ed.
C.
Gans
and
R. B.
Huey
), pp.
523
606
.
Ann Arbor, MI
:
Branta Books
.
Paukstis
,
G. L.
and
Janzen
,
F. J.
(
1990
).
Sex determination in reptiles: summary of effects of constant temperatures of incubation on sex ratios of offspring
.
Smithson. Herpetol. Info. Service
83
,
1
28
.
Peterson
,
C. R.
,
Gibson
,
A. R.
and
Dorcas
,
M. E.
(
1993
).
Snake thermal ecology: the causes and consequences of body-temperature variation
.
In Snakes – Ecology and Behavior
(ed.
R. A.
Seigel
and
J. T.
Collins
), pp.
241
314
.
New York
:
McGraw-Hill
.
Punzo
,
F.
(
1975
).
Studies on the feeding behavior, diet, nesting habits and temperature relationships of Chelydra serpentina osceola (Chelonia: Chelydridae)
.
J. Herpetol
.
9
,
207
210
.
Rhen
,
T.
and
Lang
,
J. W.
(
1995
).
Phenotypic plasticity for growth in the common snapping turtle: effects of incubation temperature, clutch and their interaction
.
Am. Nat
.
146
,
726
747
.
Rome
,
L. C.
,
Stevens
,
E. D.
and
John-Alder
,
H. B.
(
1992
).
The influence of temperature and thermal acclimation on physiological function
.
In Environmental Physiology of the Amphibians
(ed.
M. E.
Feder
and
W. W.
Burggren
), pp.
183
205
.
Chicago
:
University of Chicago Press
.
Roosenburg
,
W. M.
and
Kelley
,
K. C.
(
1996
).
The effect of egg size and incubation temperature on growth in the turtle, Malaclemys terrapin
.
J. Herpetol
.
30
,
198
204
.
Roosenburg
,
W. M.
(
1996
).
Maternal condition and nest site choice: an alternative for the maintenance of environmental sex determination?
Am. Zool
.
36
,
157
168
.
Roosenburg
,
W. M.
and
Johnson
,
C.
(
1995
).
Incubation temperature influences growth in juvenile turtles hormonally-manipulated during development
.
Am. Zool
.
35
,
89A
.
Schultz
,
E. T.
and
Warner
,
R. R.
(
1991
).
Phenotypic plasticity in life-history traits of female Thalassoma bifasciatum (Pisces: Labridae). 2. Correlation of fecundity and growth rate in comparative studies
.
Env. Biol. Fishes
30
,
333
344
.
Sedinger
,
J. S.
,
Flint
,
P. L.
and
Lindberg
,
M. S.
(
1995
).
Environmental influence on life-history traits: growth, survival and fecundity in black brant (Branta bernicla)
.
Ecology
76
,
2404
2414
.
Sinervo
,
B.
and
Adolph
,
S. C.
(
1989
).
Thermal sensitivity of growth rate in hatchling Sceloporus lizards: environmental, behavioral and genetic aspects
.
Oecologia
78
,
411
419
.
Sinervo
,
B.
and
Adolph
,
S. C.
(
1994
).
Growth plasticity and thermal opportunity in Sceloporus lizards
.
Ecology
75
,
776
790
.
Sokal
,
R. R.
and
Rohlf
,
F. J.
(
1981
).
Biometry
. (2nd edn).
New York
:
W. H. Freeman
.
Tsuji
,
J. S.
(
1988
).
Thermal acclimation of metabolism in Sceloporus lizards from different latitudes
.
Physiol. Zool
.
61
,
241
253
.
Van Damme
,
R.
,
Bauwens
,
D.
,
Braña
,
F.
and
Verheyen
,
R. F.
(
1992
).
Incubation temperature differentially affects hatching time, egg survival and hatchling performance in the lizard Podarcis muralis
.
Herpetologica
48
,
220
228
.
Viets
,
B. E.
,
Ewert
,
M. A.
,
Talent
,
L. G.
and
Nelson
,
C. E.
(
1994
).
Sex-determining mechanisms in squamate reptiles
.
J. exp. Zool
.
270
,
45
56
.
Webb
,
G. J. W.
and
Cooper-Preston
,
H.
(
1989
).
Effects of incubation temperature on crocodiles and the evolution of reptilian oviparity
.
Am. Zool
.
29
,
953
971
.
Williamson
,
L. U.
,
Spotila
,
J. R.
and
Standora
,
E. A.
(
1989
).
Growth, selected temperature and CTM of young snapping turtles, Chelydra serpentina
.
J. therm. Biol
.
14
,
33
39
.
Yntema
,
C. L.
(
1976
).
Effects of incubation temperature on sexual differentiation in the turtle, Chelydra serpentina
.
J. Morph
.
150
,
453
461
.
Yntema
,
C. L.
(
1978
).
Incubation times for eggs of the turtle Chelydra serpentina (Testudines: Chelydridae) at various temperatures
.
Herpetologica
34
,
274
277
.